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Thioalkalimicrobium Cyclicum Sp. Nov. and Thioalkalivibrio Jannaschii Sp

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Thioalkalimicrobium Cyclicum Sp. Nov. and Thioalkalivibrio Jannaschii Sp International Journal of Systematic and Evolutionary Microbiology (2002), 52, 913–920 DOI: 10.1099/ijs.0.02034-0 Thioalkalimicrobium cyclicum sp. nov. and Thioalkalivibrio jannaschii sp. nov., novel species of haloalkaliphilic, obligately chemolithoautotrophic sulfur-oxidizing bacteria from hypersaline alkaline Mono Lake (California) 1 Institute of Microbiology, Dimitry Yu. Sorokin,1,3 Vladimir M. Gorlenko,1 Tat’yana P. Tourova,1 Russian Academy of 2 2 3 Science, Prospect 60-let Alexandre I. Tsapin, Kenneth H. Nealson and Gijs J. Kuenen Octyabrya 7/2, 117811 Moscow, Russia 2 Author for correspondence: Dimitry Yu. Sorokin. Tel: j7 95 1350109. Fax: j7 95 1356530. Jet Propulsion e-mail: soroc!inmi.da.ru Laboratory/California Institute of Technology, Pasadena, CA, USA Two strains of haloalkaliphilic, obligately autotrophic, sulfur-oxidizing bacteria 3 Kluyver Institute of were isolated from the oxygen-sulfide interface water layer of stratified Biotechnology, TU Delft, T Julianalaan 67, 2628 BC alkaline and saline Mono Lake, California, USA. Strain ALM 1 was a dominant Delft, The Netherlands species in enrichment on moderate-saline, carbonate-buffered medium (06M total NaM, pH 10) with thiosulfate as an energy source and nitrate as a nitrogen source. Cells of ALM 1T are open ring-shaped and are non-motile. It has a high growth rate and activity of thiosulfate and sulfide oxidation and very low sulfur-oxidizing activity. Genetic comparison and phylogenetic analysis suggested that ALM 1T (l DSM 14477T l JCM 11371T) represents a new species of the genus Thioalkalimicrobium in the γ-Proteobacteria, for which the name Thioalkalimicrobium cyclicum sp. nov. is proposed. Another Mono Lake isolate, strain ALM 2T, dominated in enrichment on a medium containing 2 M total NaM (pH 10). It is a motile vibrio which tolerates up to 4 M NaM and produces a membrane-bound yellow pigment. Phylogenetic analysis placed ALM 2T as a member of genus Thioalkalivibrio in the γ-Proteobacteria, although its DNA hybridization with the representative strains of this genus was only about 30%. On the basis of genetic and phenotypic properties, strain ALM 2T (l DSM 14478T l JCM 11372T) is proposed as Thioalkalivibrio jannaschii sp. nov. Keywords: haloalkaliphilic sulfur-oxidizers, soda lakes, Mono Lake, Thioalkalimicrobium, Thioalkalivibrio INTRODUCTION alkaline pH are represented by saline soda lakes, and recent intensive microbiological investigation of these Colourless sulfur-oxidizing bacteria represent an im- habitats has revealed the presence of alkaliphilic portant part of microbial community in natural and bacteria belonging to various physiological groups some industrial habitats. Until recently, known sulfur- (Jones et al., 1998; Zavarzin et al., 1999). In particular, oxidizing bacteria included neutrophilic and acido- it became clear that there exists a third, halo- philic species with possible pH range for stable growth alkaliphilic, group of sulfur-oxidizing bacteria, which between 2 and 8 (Kelly, 1989; Kuenen et al., 1992). includes both heterotrophic (Sorokin et al., 1996) and Natural environments with high alkalinity and stable obligately autotrophic (Sorokin et al., 2000b) repre- ................................................................................................................................................. sentatives. Overall, more than 80 strains of alkaliphilic, Published online ahead of print on 14 December 2001 as DOI obligately autotrophic, sulfur-oxidizing strains have 10.1099/ijs.0.02034-0. been isolated and characterized (Sorokin et al., 2001a) The GenBank accession numbers for the 16S rDNA sequence of strains ALM from the volcanic soda lakes in Kenya and from the 1T and ALM 2T are AF329082 and AF329083, respectively. shallow soda lakes in dry steppes of the south-east 02034 # 2002 IUMS Printed in Great Britain 913 D. Yu. Sorokin and others Siberia and Mongolia. In general, these bacteria differ experiments. The pH influence on the activity of thiosulfate from the well-known neutrophilic species by their oxidation was tested with an oxygen electrode as described ability to grow optimally at pH " 9 and up to 10n5–10n6 previously (Sorokin et al., 2001a) using 0n1 M HEPESj in media strongly buffered by a sodium bicarbonate\ 0n6 M NaCl for the pH range 6–8 and NaHCO$\Na#CO$ carbonate mixture. All these bacteria have been buffer for higher pH values. All buffers contained 50 mM KCl. The influence of salt concentration on the activity of assigned into two new genera Thioalkalimicrobium and thiosulfate oxidation was investigated using soda buffer, pH Thioalkalivibrio in the γ-Proteobacteria (Sorokin et al., 10, with total Na+ concentration from 0n3to4M. 2001a). The two genera differ from each other in many aspects of the growth kinetics, metabolic activity and Total DNA analysis. The isolation of the DNA and sub- sequent determination of the GjC content of the DNA and genetics. In general, the genus Thioalkalimicrobium the DNA–DNA hybridization were performed according to includes fast-growing species with high activity of standard procedures (Marmur, 1961; De Ley et al., 1970). thiosulfate and sulfide oxidation but relatively low salt tolerance. Most of the strains were obtained from the Amplification and sequencing of 16S rRNA genes. For amplification and sequencing of 16S rRNA genes, the DNA low-mineralized steppe soda lakes. The genus is a was obtained by standard phenol\chloroform extraction. member of the Thiomicrospira cluster. In contrast, the The 16S rRNA genes were selectively amplified using primers genus Thioalkalivibrio is represented by the slow- 5h-AGAGTTTGATCCTGGCTCAG-3h (forward) and 5h- growing but more salt-tolerant organisms isolated TACGGTTACCT-TGTTACGACTT-3h (reverse). PCR mostly from the highly concentrated Kenyan soda products were cloned, and transformed using InvitroGene lakes. Some of the isolates were even capable of growth kit. Sequencing had been done by MWG Biotech, Inc (High in saturated soda brines. The genus Thioalkalivibrio is Point North Carolina) with Licor machine using custom- related to sulfur purple bacteria of the genus designed primers to sequence samples to an accuracy of Ectothiorhodospira (Tru$ per & Schlegel, 1964). This " 99%. A combination of both available sequencing genus also includes several strains capable of growth reactions which include dye primer on the Licor Long Read IR 4200 sequencers and dye terminator on the ABI3700 with thiocyanate as electron donor and nitrogen source capillary sequencers were used. Dye primer chemistry (Sorokin et al., 2001b) which form two new Thio- provided data read lengths from 750 to over 1100 bases, alkalivibrio species (Sorokin et al., 2002). In while the dye-terminator reaction was used to confirm base this paper we describe two new species of halo- calls and provide gap closure with read lengths ranging from alkaliphilic, obligately chemolithoautotrophic, sulfur- 500 to 750 bases. Nearly complete 16S rDNA gene sequences oxidizing bacteria isolated from the stratified, alkaline were obtained for the Mono Lake isolates ALM 1T and and saline Mono Lake in California, USA. ALM 2T (1450–1470 nucleotides). 16S rDNA sequence analysis. The sequences were aligned METHODS manually with sequences obtained from the database of small-subunit rRNAs in EMBL. The sequences were Sampling. Water samples were collected in July 1999 from compared with those of the members of the Proteobacteria. the sulfide-oxygen interface layer (depth 19–25 m) at the Regions that were not sequenced in one or more reference deepest point (48 m) of Mono Lake, California, using 5 l organism were omitted from the analyses. Pairwise evol- sampling bottles. The mean pH and total salinity values of " utionary distances (expressed as estimated changes per 100 the Mono Lake water were 9n8 and 80 g l− , respectively. The nucleotides) were computed by using the Jukes & Cantor HS− concentration decreased upwards from several hundred method. A resulting phylogenetic tree was constructed by micromolar in the anaerobic layer to several micromolar in the neighbour-joining method (Saitou & Nei, 1987) with the upper part of the interface layer. The samples were bootstrap analysis of 100 trees using programs of the brought into a laboratory within 5 h of collection and kept package (Van de Peer & De Wachter, 1994). at 4 mC until use. Bootstrap analysis (100 replications) was used to validate Media and growth conditions. Enrichment for and cul- the reproducibility of the branching pattern of the trees. tivation of aerobic alkaliphilic sulfur bacteria was per- Electron microscopy. For total preparations, cells were formed using a mineral medium strongly buffered by washed and resuspended in 0n5–1 M neutral NaCl solution, + NaHCO$\Na#CO$ (0n6–4 M total Na ) at pH 10–10n1, as pre-fixed (2 h) and then fixed (10 h) at 4 mCin0n1% and described previously (Sorokin et al., 2001a). Thiosulfate 2n5% (v\v, final) glutaralaldehyde solutions, respectively, (40–80 mM) served as the energy source and nitrate (5 mM containing the same amount NaCl, and then positively as KNO$) as the nitrogen source. Solid alkaline media with stained with 1% (w\v) uranyl acetate. For ultrathin final salt concentrations 0n6 and 2 M total Na+ were prepared sectioning cells after fixation were postfixed in 1% (w\v) by 1:1 mixing of 4% agar and double-strength mineral base OsO% solution containing 0n6–2 M NaCl for 10 h at 4 mC. at 50 mC. Enrichments for denitrifying sulfur bacteria were Then the cells were washed, dehydrated and embedded into performed
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